ORIGINAL ARTICLE

Central Auditory Development in Children

With Bilateral Cochlear Implants
Paul W. Bauer, MD; Anu Sharma, PhD; Kathryn Martin, MA, CCC-A; Michael Dorman, PhD
Objective: To examine the time course of maturation
of P1 latencies in infant sequential and simultaneous bi-
lateral cochlear implant recipients.
Design: Retrospective case series.
Setting: Pediatriccollaborativecochlear implant program.
Patients: Four children who received bilateral coch-
lear implants prior to age 2 years.
Intervention: Cortical auditory evoked potential was
completed to determine the latency of the P1 response
in 4 children with bilateral cochlear implants.
Main Outcome Measures: Longitudinal develop-
ment of the latency of the P1 cortical auditory evoked
potential in children who received bilateral cochlear im-
plants prior to age 2 years.
Results: In2patients whoreceivedsequential bilateral im-
plants, P1latenciesrecordedfromthefirstimplantedearwere
withinnormal limits after 3to6months of implant use. By
comparison, P1 latencies from the second implanted ear
reachednormal limits as earlyas 1monthafter implant use.
In2patients whoreceivedsimultaneous bilateral implants,
P1 latencies fromboth ears were also within normal limits
inaveryshort timeframe(ie, by1monthpoststimulation).
Conclusions: Our data suggest a high degree of plastic-
ity of the central auditory pathways after early bilateral
implantation. We find that P1 latencies provide a clini-
cally useful biomarker of central auditory system devel-
opment in children after cochlear implantation.
Arch Otolaryngol Head Neck Surg. 2006;132:1133-1136
B
ILATERAL PEDIATRIC COCH-
lear implantation is becom-
ing increasingly common in
clinical practice. One factor
for this is an attempt to
achieve the binaural benefit enjoyed by lis-
teners with normal hearing. The binaural
benefit includes improved performance in
noise, binaural summation, binaural
squelch, and localization of sound. These
benefits have been previously established
in adults using bilateral implants.
1-6
A motivation for and benefit of bilat-
eral implantation in young children is
to ameliorate the effects of auditory depri-
vation. It is known that speech recogni-
tion ability can become worse in the un-
aided ear for individuals who have bilateral
hearing loss but unilateral hearing aid am-
plification.
7
This deterioration is often at-
tributed to a lack of auditory stimulation
or auditory deprivation in the unaided ear.
Studies in animal models have shown that
spiral ganglion survival is decreased in the
nonstimulated ear, that intracochlear elec-
trical stimulation promotes survival of spi-
ral ganglion neurons, and that the normal
cochleotopic organization of the inferior
colliculus is severely reduced if electrical
stimulationis not initiatedat anearlyage.
8-10
In humans, the effects of auditory depri-
vation on the central auditory systemhave
beenindirectly examinedby computing P1
cortical auditory-evoked response laten-
cies as an indicator of cortical maturation
in response to sound.
11,12
The P1 response
is generated by auditory thalamic and cor-
tical sources and varies with chronologi-
cal age. Therefore, P1 latency can be used
to infer the maturational status of audi-
tory pathways after cochlear implanta-
tion.
11,13
The rapid decreases in P1 latency
after cochlear implantation are an indirect
reflection of central auditory plasticity.
Central auditory plasticity is affected by
age, with earlier age implantation associ-
ated with a shorter time interval to nor-
mal latency values for the P1 response
latency.
14-16
Demonstrating benefit from bilateral
cochlear implantation in very young chil-
dren is difficult. Computing P1 latencies
from cortical evoked responses provides
an objective measure of benefit that has
been clinically correlated with the devel-
opment of early communicative behav-
Author Affiliations:
Department of Otolaryngology,
University of Texas
Southwestern Medical Center,
Dallas (Dr Bauer); Department
of Behavioral and Brain Science,
Callier Advanced Hearing
Research Center, University of
Texas at Dallas (Dr Sharma and
Ms Martin); and Department of
Speech and Hearing Science,
Arizona State University, Tempe
(Dr Dorman). Dr Bauer is now
with the Department of
Pediatric Otolaryngology,
Medical City Childrens
Hospital, Dallas. Dr Sharma is
now with the Department of
Speech, Language, and Hearing
Science, University of Colorado
at Boulder.
(REPRINTED) ARCH OTOLARYNGOL HEAD NECK SURG/ VOL 132, OCT 2006 WWW.ARCHOTO.COM
1133
2006 American Medical Association. All rights reserved.
at Univ of Colorado Hlth Sci Ctr, on March 6, 2007 www.archoto.com Downloaded from
iors.
16
We report results from 4 children who under-
went bilateral implantation before the age of 2 years. Two
of these children were fitted with implants sequentially,
and the other 2 received their bilateral implants simul-
taneously. The P1 response latencies were recorded at
various time intervals following implantation to assess
the effects of bilateral implantation on the maturation of
the central auditory pathways.
METHODS
Four children undergoing bilateral cochlear implantation be-
tween the ages of 12 to 24 months were identified, and their
cortical evoked responses were reviewed in retrospect. Medi-
cal charts were reviewed to identify the etiology of hearing loss,
time course and experience with hearing aids, and timing of
cochlear implantation as these factors relate to the intervals of
cortical evoked response testing. This research was approved
by the institutional review boards of the University of Texas
SouthwesternMedical Center, Dallas, andthe University of Texas
at Dallas.
Cortical auditory-evoked responses were recorded in re-
sponse to a synthesized speech syllable /ba/. Full information on
the stimulus has been previously published.
17
The stimulus was
presented via a loudspeaker placed at an angle of 45 to the im-
planted side. Processors were set to the childrens usual proces-
sor settings. Subjects were seated comfortably ina reclining chair
placed in a sound booth. Subjects watched a videotaped movie
or cartoon of their choice on a television monitor placed in front
of them in the sound booth. Videotape audio levels were kept
belowa 45-dB sound pressure level. Evoked potentials were col-
lected using Cz as the active electrode (Cz refers to the vertex
midline placement). The reference electrode was placed on the
mastoid and a ground electrode on the forehead. On some of the
children with bilateral implants, the P1 response was obscured
by the presence of a stimulus artifact in the first 100 ms of the
recording. Inthese cases, the reference electrode was movedalong
the isopotential field of the artifact (typically around the fore-
head) to a point of null polarity, where the amplitude of the ar-
tifact was minimal and the response could be easily visual-
ized.
18
Eye movements were monitored using a bipolar electrode
montage (lateral outer canthus to superior outer canthus). The
reference electrodes were placed onthe mastoids. Averaging was
automatically suspended by the recording computer when eye
blinks were detected. The recording windowincluded a 100-ms
prestimulus time and600-ms poststimulus time. Incomingevoked
responses were analog filtered from 0.1 to 100 Hz. Approxi-
mately 300 response sweeps were collected for each subject. The
test session, including electrode application and evoked re-
sponse recording, lasted for about 30 minutes. Sweeps greater
than 100 V were rejected off-line, and the remaining sweeps
were averaged to compute a grand average waveformfor the in-
dividual subjects. We defined P1 as the first robust positivity in
the auditory evoked potential waveform in the 50- to 175-ms
range.
17
The P1 latency was labeled at the peak of the response
or, if the peak was broad, at the midpoint. The P1 response la-
tencies were plotted against the 95%confidence interval for nor-
mal development of the P1 response.
17
RESULTS
Patient 1 has asymptomatic congenital cytomegalovirus
infection as the etiology to her profound sensorineural
hearing loss. Whenthe patient was tested at age 8 months,
the results of auditory brainstemresponse testing showed
a profoundhearing loss bilaterally. Aidedthresholds tested
in a sound field revealed a pure-tone average (PTA) of
90-dB hearing level (HL). Patient 1 met the criteria for
cochlear implantation and underwent implantation in the
left ear at age 12 months and in the right ear at age 24
months. The postimplantation developmental trajec-
tory for P1 latencies is shown in the Figure, A. At the
time of hook-up in the left ear, the P1 latency was sig-
nificantly delayed, which is indicative of an unstimu-
latedauditory system.
13
Consistent withour previous find-
ings, as experience with the implant increased, rapid
decreases in P1 latency were observed, and the P1 re-
sponse latency was within normal limits after 3 months
of implant use.
13
At the time of initiation of stimulation
of the second (right) ear, the P1 latency was less de-
layed compared with the hook-up latency of the first ear.
The P1 latency in the second ear reached normal limits
within a month of initial stimulation. When tested at age
3years, P1 latencies fromboth ears continued to show
normal development.
Patient 2 has GJB2 (connexin 26 and 30) mutations
(312del14 and del342kb) as the etiology to his pro-
found sensorineural hearing loss. Behavioral testing re-
vealed unaided and aided thresholds in the severe to pro-
found hearing loss range. Patient 2 underwent cochlear
implantation in the left ear at age 10 months and in the
right ear at age 15 months. The developmental trajec-
tory for the P1 response is shown in the Figure, B. At the
time of hook-up in the left ear, consistent with the pro-
found hearing loss, the P1 latency was significantly de-
layed. Unfortunately, no data points could be obtained
in this ear until 6 months poststimulation, at which time
the P1 latency was well withinnormal limits. The hook-up
data point of the right ear was contaminated by an arti-
fact; however, we were able to infer a latency value that
was less delayed compared to the hook-up latency for the
first ear. The P1 latency in the right ear continued to de-
crease as expected, and when tested at age 1and at age
2 years, the P1 latency from both ears was developing
normally.
Patient 3 has asymptomatic congenital cytomegalo-
virus infection as the etiology of her profound sensori-
neural hearing loss. Behavioral testing showed that she
had an unaided PTA of 98-dB HL in the right ear and
105-dB HL in the left ear. The aided PTA was 75-dB HL
when tested in the sound field. Patient 3 met the stan-
dard candidacy criteria for cochlear implantation and un-
derwent simultaneous bilateral implantation at age 12
months. The developmental trajectory for the P1 re-
sponse latency is shown in the Figure, C. In this case,
although the P1 latencies from both ears were signifi-
cantly delayed at the time of activation, the latencies from
both ears were within normal limits as early as 1 month
after initial stimulation.
Patient 4 has congenital severe-profound sensorineu-
ral hearing loss. Behavioral testing showed that his un-
aided PTAs were 78-dB HL in the right ear and 83-dB HL
in the left ear. His aided PTA was 53-dB HL when tested
in the sound field. He underwent simultaneous bilateral
cochlear implantation at age 15 months. The develop-
mental trajectory of the P1 response is shown in the
Figure, D. At hook-up, P1 latencies from both ears were
(REPRINTED) ARCH OTOLARYNGOL HEAD NECK SURG/ VOL 132, OCT 2006 WWW.ARCHOTO.COM
1134
2006 American Medical Association. All rights reserved.
at Univ of Colorado Hlth Sci Ctr, on March 6, 2007 www.archoto.com Downloaded from
delayed. The delay in P1 latencies is less than that seen
for patients 1, 2, and 3, consistent with the fact that this
childhadbetter aidedthresholds thanthose children. That
is, P1 latencies in this patient reflected auditory path-
ways that had received some (albeit not enough) degree
of stimulation with hearing aids. After implantation, P1
latencies reached normal limits bilaterally after 1 month
of implant use. As shown in the Figure, D, P1 latencies
continued to show normal development after 7 months
of implant use.
COMMENT
We have described the time course of maturation of the
central auditory pathways (as reflected by P1 latencies)
in4 patients who receivedbilateral cochlear implants early
in life (ie, younger than 2 years). In the 2 patients who
received sequential implants, P1 latencies recorded from
the first implanted ear were within normal limits after 3
to 6 months of implant use. This result is consistent with
the trajectory for P1 latency development in children who
are fitted with a unilateral cochlear implant at an early
age.
14
For the sequentially implanted children, the P1 la-
tency from their second implanted ear was less delayed
at hook-up than the P1 latency from their first im-
planted ear. This finding is consistent with brain imag-
ing and current source density data in both animal and
human models that showa robust contralateral and weak
ipsilateral stimulation (crossed and uncrossed fibers of
the central auditory pathways) after unilateral implan-
tation.
19
Therefore, it is perhaps not surprising that the
P1 latencies in the second implanted ear are within nor-
mal limits by about 1 month after stimulation because
they have a shorter distance to travel.
To our knowledge, this study presents for the first time
trajectories for P1 latency development in young children
whowere fittedwithbilateral implants simultaneously. We
wouldpredict that the P1latency inour simultaneous early
implant recipients shouldnormalize alonga trajectorysimi-
lar to other unilateral early implant recipients (or, in the
case of our patients, the first ear of the sequential implant
recipients). However, in our patients who received simul-
500
400
300
200
100
0 1 2 3 4 5
Age, y
Hook-up
1 wk
1 mo
Hook-up
Hook-up
Hook-up
Hook-up
1 wk
1 mo
7 mo
1 wk
1 mo 6 mo
10 mo
5 mo
1 wk
3 mo
12 mo
1 mo
19 mo
31 mo
P
1

L
a
t
e
n
c
y
,

m
s
Hook-up
1 mo
7 mo
Left Ear
Right Ear
A
500
400
300
200
100
0 1 2 3 4 5
Age, y
P
1

L
a
t
e
n
c
y
,

m
s
B
500
400
300
200
100
0 1 2 3 4 5
Age, y
P
1

L
a
t
e
n
c
y
,

m
s
C
400
300
200
100
0 1 2 3 4 5
Age, y
P
1

L
a
t
e
n
c
y
,

m
s
D
Normal Limits Normal Limits
Normal Limits Normal Limits
Figure. Trajectories for P1 latency changes following sequential bilateral implantation for (A) patient 1, (B) patient 2, (C) patient 3, and (D) patient 4. The solid
lines represent the 95% confidence intervals for normal development of P1 latencies.
(REPRINTED) ARCH OTOLARYNGOL HEAD NECK SURG/ VOL 132, OCT 2006 WWW.ARCHOTO.COM
1135
2006 American Medical Association. All rights reserved.
at Univ of Colorado Hlth Sci Ctr, on March 6, 2007 www.archoto.com Downloaded from
taneous earlybilateral cochlear implants, the P1latencywas
near normal limits by 1monthafter implantation. This was
most pronouncedinpatient 3, inwhomthe P1 latency was
significantly delayed at the time of initial hook-up. Why
was the time interval to a normal P1 latency so brief in pa-
tient 3? Although to our knowledge there are no animal
models or other human studies to provide insight to this
question, it is likely that simultaneous early implantation
creates anenvironment inwhichboththe crossed and un-
crossedfibers of the central auditory systemona givenside
are being simultaneously stimulated. We theorize that syn-
ergistic (ipsilateral and contralateral) stimulation facili-
tates rapid development of central auditory pathways.
In conclusion, our data suggest a high degree of plas-
ticity of the central auditory pathways after early bilat-
eral implantation. These results support early bilateral
implantation to preserve the integrity of the central au-
ditory system. Finally, we found that P1 latencies pro-
vide a clinically useful biomarker of central auditory de-
velopment in young children who undergo cochlear
implantation.
Submittedfor Publication: March28, 2006; acceptedMay
7, 2006.
Correspondence: Paul W. Bauer, MD, Department of Pe-
diatric Otolaryngology, Medical City Childrens Hospi-
tal, 7777 Forest Ln, Suite C-706, Dallas, TX75230 (bauer
@entforchildren.net).
Author Contributions: The authors had full access to all
the data in the study and take responsibility for the in-
tegrity of the data and the accuracy of the data analysis.
Study concept and design: Bauer, Sharma, and Dorman.
Acquisition of data: Bauer, Sharma, and Martin. Analysis
and interpretation of data: Bauer, Sharma, and Dorman.
Drafting of the manuscript: Bauer, Sharma, and Dorman.
Critical revision of the manuscript for important intellec-
tual content: Bauer, Sharma, Martin, and Dorman. Sta-
tistical analysis: Sharma. Obtained funding: Sharma. Ad-
ministrative, technical, and material support: Bauer, Sharma,
Martin, andDorman. Study supervision: Bauer andSharma.
Financial Disclosure: None reported.
Funding/Support: This study was supported by the Na-
tional Institutes of Health grants NIDCDR01 DC006257
and NIDCD R01 DC004552.
Previous Presentation: This study was presented in part
at the Tenth Symposium on Cochlear Implants in Chil-
dren; March 16, 2005; Dallas, Tex.
REFERENCES
1. Muller J, Schon F, Helms J. Speech understanding in quiet and noise in bilateral
users of the MED-EL COMBI 40/40cochlear implant system. Ear Hear. 2002;
23:198-206.
2. Nopp P, Schleich P, DHaese P. Sound localization in bilateral users of MED-EL
COMBI 40/40 cochlear implants. Ear Hear. 2004;25:205-214.
3. Schleich P, Nopp P, DHaese P. Head shadow, squelch, and summation effects
in bilateral users of the MED-EL COMBI 40/40cochlear implant. Ear Hear. 2004;
25:197-204.
4. Schon F, Muller J, Helms J. Speech reception thresholds obtained in a sym-
metrical four-loudspeaker arrangement from bilateral users of MED-EL coch-
lear implants. Otol Neurotol. 2002;23:710-714.
5. Van Hoesel R, Ramsden R, Odriscoll M. Sound-direction identification, interau-
ral time delay discrimination, and speech intelligibility advantages in noise for a
bilateral cochlear implant user. Ear Hear. 2002;23:137-149.
6. Van Hoesel RJ. Exploring the benefits of bilateral cochlear implants. Audiol
Neurootol. 2004;9:234-246.
7. Gelfand SA, Silman S. Apparent auditory deprivation in children: implications of
monaural versus binaural amplification. J Am Acad Audiol. 1993;4:313-318.
8. Leake PA, Hradek GT, Snyder RL. Chronic electrical stimulation by a cochlear
implant promotes survival of spiral ganglion neurons after neonatal deafness.
J Comp Neurol. 1999;412:543-562.
9. Leake PA, Snyder RL, Rebscher SJ, Moore CM, Vollmer M. Plasticity in central
representations in the inferior colliculus induced by chronic single- vs two-
channel electrical stimulation by a cochlear implant after neonatal deafness. Hear
Res. 2000;147:221-241.
10. Moore CM, Vollmer M, Leake PA, Snyder RL, Rebscher SJ. The effects of chronic
intracochlear electrical stimulation on inferior colliculus spatial representation
in adult deafened cats. Hear Res. 2002;164:82-96.
11. Sharma A, Dorman M, Kral A. The influence of a sensitive period on central au-
ditory development in children with unilateral and bilateral cochlear implants. Hear
Res. 2005;203:134-143.
12. Ponton CW, Don M, Eggermont JJ, et al. Maturation of human cortical auditory
function: differences between normal hearing children and children with coch-
lear implants. Ear Hear. 1996;17:430-437.
13. Sharma A, Martin K, Roland P, et al. P1 latency as a biomarker of central audi-
tory development in children with hearing impairment. J Am Acad Audiol. 2005;
16:564-573.
14. Sharma A, Dorman MF, Spahr AJ. Rapid development of cortical auditory evoked
potentials after early cochlear implantation. Neuroreport. 2002;13:1365-1368.
15. Sharma A, Dorman M, Spahr A, Todd NW. Early cochlear implantation in chil-
dren allows normal development of central auditory pathways. Ann Otol Rhinol
Laryngol Suppl. 2002;189:38-41.
16. Sharma A, Tobey E, Dorman M, et al. Central auditory maturation and babbling
development in infants with cochlear implants. Arch Otolaryngol Head Neck Surg.
2004;130:511-516.
17. Sharma A, Dorman M, Spahr AJ. A sensitive period for the development of the
central auditory system in children with cochlear implants: implications for age
of implantation. Ear Hear. 2002;23:532-539.
18. Gilley PM, Sharma A, Dorman M, Finley CC, Panch AS, Martin K. Minimization
of cochlear implant stimulus artifact in cortical auditory evoked potentials. Clin
Neurophysiol. 2006;117:1772-1782.
19. Roland PS, Tobey EA, Devous MD Sr. Preoperative functional assessment of au-
ditory cortex in adult cochlear implant users. Laryngoscope. 2001;111:77-83.
(REPRINTED) ARCH OTOLARYNGOL HEAD NECK SURG/ VOL 132, OCT 2006 WWW.ARCHOTO.COM
1136
2006 American Medical Association. All rights reserved.
at Univ of Colorado Hlth Sci Ctr, on March 6, 2007 www.archoto.com Downloaded from